Clinical Experience of Lobectomy With Pulmonary Artery Reconstruction for Central Non–Small-Cell Lung Cancer

Original Study

Clinical Experience of Lobectomy With Pulmonary Artery Reconstruction for Central Non–Small-Cell Lung Cancer Rong Yin,1 Lin Xu,1 Binhui Ren,1 Feng Jiang,1 Xiaohu Fan,2 Zhi Zhang,1 Ming Li,1 Zhendong Hu1 Abstract Background: In patients with central lung cancer, lobectomy can be achieved without pneumonectomy by surgical reconstruction of the pulmonary artery (PA). Herein, we report our clinical experience of 34 patients who had lobectomy with PA reconstruction, including perioperative administration, morbidity, mortality, and long-term survival. Patients and Methods: The clinical records of 34 patients who received lobectomy with PA reconstruction in our department between August 2003 and September 2005 were reviewed. Results: In our series, PA reconstruction with endto-end anastomosis was performed in 18 patients (52.9%). Seven patients (20.6%) required partial PA reconstruction with autologous pericardium patch. Five patients (14.7%) with a lower lobe tumor required PA reconstruction with artery flap. The perioperative mortality was 2.9%, and 1 patient died on postoperative day 13 because of severe bronchopleural fistula. Another 2 patients had acute respiratory distress syndrome (ARDS) and required reintubation in our Intensive Care Unit. The overall Kaplan-Meier 3-year and 5-year survival rates were 46% and 37%, respectively. As compared with the stage III patients, stage I patients had significantly greater 5-year survival (80% vs. 11%; P = .005). Patients with pN0 disease also had greater 5-year survival than patients with pN2-3 disease (71% vs. 9%; P = .004). Conclusion: In our department, PA reconstruction has been more frequently and actively performed for patients with central lung cancer, especially for some patients with a lower lobe tumor. Although the morbidity and mortality is acceptable, surgeons should be more attentive to lethal postoperative complications such as ARDS induced by lung ischemia-reperfusion injury. Clinical Lung Cancer, Vol. 11, No. 2, 120-125, 2010; DOI: 10.3816/CLC.2010.n.016 Keywords: Acute respiratory distress syndrome, Anastomosis, Atrial fibrillation, Pulmonary vein graft

Introduction Non–small-cell lung cancer (NSCLC) remains the leading cause of cancer deaths worldwide.1 Central lung cancer is usually considered a contraindication to surgical resection.2 Current development of surgical techniques such as bronchovascular sleeve resection,3 pulmonary artery (PA) reconstruction,4 and lung autotransplantation5 provide the possibility of achieving a margin-negative (R0) resection and without pneumonectomy (PN) for patients with central lung cancer. Recent meta-analyses have demonstrated that bronchial or bronchovascular sleeve resection offers a better long

1Department

of Thoracic Surgery, Cancer Hospital of Jiangsu Province, Cancer Institution of Jiangsu Province, Nanjing, China 2Department of Pediatrics, University of Alberta, Edmonton, Canada



Submitted: Aug 25, 2009; Revised: Nov 24, 2009; Accepted: Dec 10, 2009



Address for correspondence: Lin Xu, MD, Department of Thoracic Surgery, Cancer Hospital of Jiangsu Province, 42 Baiziting, Nanjing, 210009, China Fax: 86-25-8364-1062; e-mail: [email protected]



term survival rate with no increase in morbidity and mortality compared with that of PN.6 Therefore, if a patient’s tumor is considered “resectable” (and he/she cannot tolerate PN), it is valuable to examine the possible application of these techniques. Since the 1990s, when Rendina and colleagues7,8 confirmed the feasibility and value of PA reconstruction, various techniques such as end-to-end anastomosis; pericardial patch4; pericardial, prosthetic,7 or heterologous conduit9; and autologous pulmonary vein (PV) graft10 were gradually developed and performed. In this study, we reviewed our clinical experience of lobectomy with partial and circumferential PA reconstruction for the treatment of central NSCLC. We performed this technique frequently and actively, especially for patients with lower lobe tumors that infiltrated the inferior aspect of interlobar PA.

Patients and Methods This retrospective study was approved by our hospital’s Ethics Committee. We reviewed the clinical records of all the patients

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Figure 1 Schematic Diagram of Left Lower Lobe Neoplasm Invading Inferior Aspect of Pulmonary Artery and Reconstruction With Artery Flap A

B

Lingular Artery

C

Artery Flap

Tumor

(A) Left lower lobe tumor invading inferior aspect of pulmonary artery. (B) After resection. (C) After reconstruction with artery flap. Abbreviation: PA = pulmonary artery

with central NSCLC who had undergone an R0 lobectomy with partial and circumferential PA reconstruction (all the margins were confirmed negative by frozen section immediately during the operation) from August 2003 to September 2005 in the Thoracic Surgery Department; Cancer Hospital of Jiangsu Province; Nanjing, China. All the operations were performed by one surgeon (Dr. Lin Xu). The definition of PA reconstruction is similar to that previously described,4 and the procedures for clamping the PA for operative safety are not included. Perioperative mortality was defined including all in-hospital deaths and deaths occurring within 30 days of surgery. Postoperative adjuvant chemotherapy (carboplatin and paclitaxel) was administered to all 34 patients.

Figure 2 Typical Computed Tomography Scan of a Patient With a Left Lower Lobe Tumor Infiltrating the Inferior Aspect of Lingular Artery

Preoperative Evaluation For all patients, preoperative evaluations included clinical history, physical examination, routine blood tests, artery blood gas analysis, electrocardiographic analysis, and lung function tests. The lung cancer staging protocol included chest radiographic analysis, fiberoptic bronchoscopy, isotopic bone scanning, and thoracic, upper abdominal, and cerebral computed tomography (CT). Surgical treatment was considered functionally possible if the forced expiratory volume in 1 second (FEV1) was > 40% of predicted value and there was no major hypoxemia (PO2 < 60 mmHg) or hypercapnia (PCO2 > 50 mm Hg) existed. In particular, if FEV1 was between 30% and 40% (usually diagnosed as a severe obstructive pulmonary dysfunction [OPD]), an eventual operative decision was made based on full evaluation including artery blood gas analysis, age, Karnofsky Performance Scale score, cardiac function, and the results of a stair climbing exercise. In cases where N2 disease was clinically suspected (short axis > 1 cm at CT scan), fluorodeoxyglucose positron emission tomography (FDG-PET) scans were usually performed instead of mediastinoscopy, which was unavailable at our hospital until the end of 2006. Also, if PET scans indicated a high possibility of N2 lymph node metastasis, neoadjuvant chemotherapy was administered. Patients were then considered operable in the presence of a clinical response or stable disease. In progressive cases of disease, surgical intervention was denied.

Abbreviation: PA = pulmonary artery

Surgical Technique Operations were performed under general anesthesia with double-lumen endobronchial intubation. PA reconstruction was considered when conventional, safe dissection of PA branches could not be performed and a lobectomy could still yield complete resection of the tumor. The PV of the lobe to be removed was first dissected and divided by a stapler. Then heparin (3125 U) was administrated intravenously about 1 minute before vessel occlusion. In the event of proximal PA occlusion, on the left side and if only the interlobar PA was invaded, the PA trunk can be extrapericardially clamped just distal to the ligamentous arteriosis. In particular, careful attention to avoid the left recurrent laryngeal nerve is important. If the artery is infiltrated close to its origin, the pericardium must then be opened and proximal PA occlusion can be obtained intrapericardially. On the right side, if the tumor infiltrated very proximally, the anatomy of this region determined whether PN was usually unavoidable because of the invasion of the superior vena cava (SVC) or right atrium. Therefore proximal PA clamping was usually obtained

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Pulmonary Artery Reconstruction for Central Lung Cancer Table 2 Surgical Data

Table 1 Patient Characteristics Characteristic Mean Age, Years (Range)

Number of Patients (%) 56.7 ± 11.3 (34-78)

Sex Male

21 (62)

Female

13 (38)

Smokers

24 (71)

Neoadjuvant Chemotherapy

4 (11.8)

Preoperative FEV1%

50.1% ± 10.3%

Histology Squamous cell carcinoma

21 (61.3)

Adenocarcinoma

8 (23.5)

Adenosquamous carcinoma

5 (15.2)

pTNM Stage I: T1N0 = 1; T2N0 = 4

5 (14.7)

II: T1N1 = 2; T2N1 = 9; T3N0 = 2

13 (38.2)

IIIA: T1N2 = 3; T2N2 = 6; T3N1 = 3; T3N2 = 1

13 (38.2)

IIIB: T2N3 = 1; T4N1 = 1; T4N2 = 1

extrapericardially. Furthermore, as described by Rendina7,8 and Cerfolio,4 the distal of the PA was not occluded and backflow was avoided by occlusion of PV of the reserved lobe. Subsequently, PA resection and reconstruction was carried out. If sleeve resection of the bronchus and artery were both required, bronchial resection was usually obtained first and an intercostal muscle flap was used to prevent a bronchopleural fistula as previously described.3 End-to-end anastomosis, direct suturing, and pericardium patch reconstruction with 5-0 Prolene (Ethicon, Inc.; Somerville, NJ) were the most frequently used methods for PA reconstruction. When the defect PA was removed, it was necessary to examine the PA from the inside to determine whether a partial or circumferential reconstruction was needed. If the removed PA was not large enough to narrow the PA lumen more than 20% after suturing, suturing was usually chosen directly. Otherwise, circumferential resection and end-to-end anastomosis were performed. An alternative was an autologous pericardium patch. In this case, we recommended preparing it before pulmonary vessel occlusion in order to reduce the clamping time. During suturing, the PA anastomotic site was washed with heparin solution (12,500 U heparin in 500 mL normal saline, at room temperature) to prevent intraluminal thrombosis. In particular, when tumors were present in the left lower lobe infiltrating the inferior aspect of the lingular artery, as shown in Figures 1 and 2, the interlobar artery was then incised obliquely. If the superior aspect of interlobar artery has sufficient area, we preferred to use it as an artery flap and suture it to the inferior edge of the PA. Thus, the pericardium or prosthetic patch was made unnecessary, saving valuable clamping time. Finally, the distal clamp of the PV was released before tying the sutures. After ensuring the hemostasis of the PA, the proximal clamp was removed to restore the pulmonary circulation.

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Value

Location of Tumors Left upper

18 (52.9%)

Left lower

7 (20.6%)

Right upper

4 (11.8%)

Right middle

2 (5.9%)

Right lower

3 (8.8%)

Operative Procedures Partial PA reconstruction with direct suturing

4 (11.8%)

Partial PA reconstruction with pericardium patch

7 (20.6%)

Circumferential PA reconstruction with end-to-end anastomosis

18 (52.9%)

PA reconstruction with artery flap

5 (14.7%)

Bronchovascular double-sleeve resection

20 (58.8%)

Mean Occlusion Time of PA, Min

50.6 ± 12.8

Mean Occlusion Time of PV, Min

45.9 ± 11.5

Abbreviations: PA = pulmonary artery; PV = pulmonary vein

3 (8.8)

Abbreviations: FEV1 = forced expiratory volume in 1 second; pTNM = pathologic tumornode-metastasis

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Surgical Characteristic

Postoperative Care No further anticoagulant therapy was administrated postoperatively. The administration of intravenous fluids was also minimized to avoid volume overload and the possibility of pulmonary edema. Pain control was achieved in most cases by continuous patientcontrolled intravenous analgesia with tramadol or morphinics. Appropriate antibiotic coverage for 3-5 days was also necessary. For the patients who underwent bronchovascular double-sleeve resection, bronchial drainage was supported to improve coughing whenever necessary. Before being discharged from the hospital, the airway anastomosis of all patients was reconfirmed by using flexible surveillance bronchoscopy.

Follow-up Patients were followed up after resection, including chest and abdominal CT, and bronchoscopy every 3 months for the first 2 years and every 6 months from then on. Follow-up was completed up to May 2009 or to the date of death. Data were obtained from multiple sources: clinic letters, follow-up scans, hospital computer information systems, telephone calls, and letters from oncologists and other physicians.

Statistical Analysis Results are presented as mean ± SD. Kaplan-Meier survival curves were performed with SPSS for Windows (version 13.0.1, SPSS Inc, Chicago, IL). Differences among curves were analyzed by the log-rank test. A P value of ≤ .05 was considered significant.

Results Patient Profile Between August 2003 and September 2005, 34 of 738 patients (4.6%) who received lobectomy required PA reconstruction as described to avoid PN. Clinical profiles of all patients are summarized

Rong Yin et al Figure 4 Survival Analysis According to Pathologic TNM Staging

Table 3 Perioperative Morbidity and Mortality Value

Morbidity Measure, n (%)

100 90

ARDS (Reintubation)

2 (5.9)

Bronchopleural Fistula

2 (5.9)

Persistent Air Leakage

3 (8.8)

Atelectasis

2 (5.9)

Atrial Fibrillation

7 (20.6)

Left Recurrent Laryngeal Nerve Neurapraxia

1 (2.9)

30

Perioperative Mortality

1 (2.9)

20

80%

80

Survival, %

70 50 40

10

Abbreviation: ARDS = acute respiratory distress syndrome

55%

60

0

Stage I Stage II Stage III 12

11%

24

36

48

60

72

Time, Months

Figure 3 The Overall Kaplan-Meier 3-Year and 5-Year Survival Rate

Abbreviation: TNM = tumor-node-metastasis

100

Figure 5 Survival Analysis According to Pathologic N Staging

90 80

100 90

60

80

46%

50 40 30 20 10

60 50

12

24

36

48

60

72

Time, Months

in Table 1. All patients were staged according to the pathologic TNM classification (6th edition of American Joint Committee for Cancer Staging). Four patients (11.8%) who were diagnosed clinically N2 by FDG-PET accepted neoadjuvant chemotherapy preoperatively. There were 5 stage I patients (14.7%), 13 stage II patients (38.2%), 13 stage IIIA patients (38.2%), and 3 stage IIIB patients (8.8%). T4 stage included involvement of recurrent laryngeal nerve and trachea (n = 1 respectively). The proportion of patients diagnosed with squamous cell carcinoma (61.3%) was greater than other types of NSCLC.

Surgical Data Table 2 lists the surgical data of all patients. Eighteen upper left (52.9%), 7 lower left (20.6%), 4 upper right (11.8%), 2 middle right (5.9%), and 3 lower right tumors (8.8%) were located. PA reconstruction with end-to-end anastomosis was performed in eighteen patients (52.9%). Seven patients (20.6%) required partial PA reconstruction with autologous pericardium patch. No prosthetic patches were used in our series. Five patients (14.7%; 4 lower left and 1 lower right) underwent PA reconstruction with artery flap as described in Figure 1. Twenty (58.8%) of 34 patients underwent bronchial sleeve resection simultaneously. The mean occlusion time of the PA and PV was 50.6 ± 12.8 and 45.9 ± 11.5 minutes, respectively.

43%

40 30

0

71%

70

37%

Survival, %

Survival, %

70

10

pN Stage N0 N1 N2-3

0

12

20

9% 24

36

48

60

72

Time, Months

Perioperative Morbidity and Mortality There was no intraoperative mortality (Table 3). Atrial fibrillation was the most frequent postoperative complication (7 of 34; 20.6%). The perioperative mortality was 2.9% and 1 patient died on postoperative day 13 because of multiple organ dysfunction syndrome (MODS) induced by severe bronchopleural fistula. Two patients with acute respiratory distress syndrome (ARDS) were reintubated on postoperative days 2 and 3, respectively. Chest X-rays revealed typical “ground-glass opacity” and pulmonary edema. One of these two patients subsequently confirmed (by bronchoscope) a bronchopleural fistula on day 6 and pneumonectomy was performed on day 8. Furthermore, although anticoagulant therapy was not administrated postoperatively, there were no signs of pulmonary thrombosis or embolism. Other complications include air leakage, atelectasis, and left recurrent laryngeal nerve neurapraxia.

Survival No patient was lost during follow-up. Median follow-up time was 32 months, ranging from 6 to 70 months. Figures 3-6 shows the overall survival curve and survival analysis according to TNM stage, pN stage, and different surgical procedures, respectively. The

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Pulmonary Artery Reconstruction for Central Lung Cancer Figure 6 Survival Rate Between Patient Receiving Pulmonary Reconstruction Only (PA) and Bronchovascular Double-Sleeve Resection (PA + BP) 100 90 80

Survival, %

70 60 50

42%

40 30 20 10 0

33% Surgical Procedure PA only PA + BP 12

24

36

48

60

72

Time, Months Abbreviations: BP = bronchoplasty; PA = pulmonary artery reconstruction

overall Kaplan-Meier 3-year and 5-year survival rate was 46% and 37%, respectively (Figure 3). As compared with stage III patients, stage I patients had a significantly greater 5-year survival (80% vs. 11%; P = .005; Figure 4). Similarly, patients with pN0 also had a greater 5-year survival rate than patients with pN2-3 (71% vs. 9%; P = .004; Figure 5). However, there was no significant difference between patients who underwent PA reconstruction only and bronchovascular double-sleeve resection (42% vs. 33%; P = .821; Figure 6). In addition, the 5-year rate of locoregional and distant recurrence was 9 of 34 (26.5%) and 12 of 34 (35.3%), respectively.

Discussion Currently, lobectomy with PA reconstruction has been widely accepted by most lung caner surgeons. In a study previously conducted by our department,11 21 of 78 patients underwent PA reconstruction between 1976 and 1995. At that time, direct occlusion of proximal and distal PA was still the primary technique used in PA reconstruction. In the current study, we modified this technique and occluded the reserved PV instead of distal PA based on the description by Rendina et al.7,8 As compared with a simple PA occlusion, clamping the distal reserved PV can provide clearer surgical vision, greater operative space, simpler procedures, and safer margin. We therefore applied this technique actively and frequently. The present data indicates that our series of 34 patients had acceptable complications and a good 5-year survival rate. In previous studies, PA reconstruction seems to have been more prevalent for patients with left-side and upper lobe tumors.4 However, in our series, more (29.4%) patients with lower lobe tumors (7 left and 3 right) required artery reconstruction. In these cases, the inferior aspect of interlobar artery was usually involved, the tumor arising in the lower lobe or infiltrative metastatic lymph nodes, as shown in Figure 1. The neoplastic invasion was usually extended longitudinally and the anterior aspect of the interlobar artery was tumor free. Therefore, if there was sufficient area of artery, we could use it as a vessel flap. Compared with pericardial patch reconstruction, this technique may save some time and surgical procedures. Five patients (14.7%) received artery flap reconstruction. Postop-

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erative radioisotope scanning displayed strong perfusion in the reserved lobe and no patients suffered from a pulmonary embolism or thrombosis, proving that this technique is safe. Moreover, in agreement with Dr. Rendina’s7 viewpoint, we also prefer the sleeve PA resection and end-to-end anastomosis rather than pericardial patch. The exceedingly long pericardial patch might induce kinking of the vessel and impairment of blood flow, especially in the upper lobe. As such, we only performed 7 (20.6%) cases of pericardial patch reconstruction including 5 patients with tumors in the lower lobe. Anticoagulant therapy for patients who have PA reconstruction remains controversial. Rendina et al7 administrated 3000-5000 U intraoperative heparin and 15000 U subcutaneously for the first postoperative week. Cerfolio et al4 recommended a lower dose (1500 U) of intraoperative heparin and no further postoperative anticoagulation therapy. Alifano et al12 only used perioperative low-molecular-weight heparin at preventive doses and no intraor postoperative heparin was administrated. In our experience, we considered 3125 U intraoperative heparin to be safe (did not increase the risk of bleeding). Although we did not have any comparative data until now, it seems unnecessary to administer postoperative anticoagulation drugs because it is also nonstandard routine for patients with congenial heart diseases accepting PA repair with or without pericardial patch under cardiopulmonary bypass. In our series, the overall 5-year survival was 37%, which was lower than that of Cerfolio et al (60%),4 Rendina et al (38.3%),7 and Lausberg et al (42.9%),3 but slightly higher than our previously reported 33.3%.11 In the stage I and pN0 group, the 5-year survival was 80% and 71% and dramatically higher than the 11% of stage III patients and 9% of pN2. According to previous studies,13-15 the 5-year survival rate of patients who required pneumonectomy was usually < 30%. Therefore, when the defective PA is resectable, it is worthwhile to perform a lobectomy with PA reconstruction to avoid pneumonectomy, especially for the patients in earlier stages. Our data and experience once again indicate that this technique is safe and does not compromise or violate oncologic principles. Finally, although this technique is gradually maturing worldwide, surgeons remain attentive to some of the severe postoperative complications. After all, this technique takes a significant amount of time and effort. For an instant, the exceedingly long occlusion time of pulmonary vessels will induce serious lung ischemia-reperfusion injury. A time duration of 1 hour is usually sufficiently long for most surgeons to finish PA reconstruction. However, 2 patients suffered from ARDS and were reintubated postoperatively in our series. Their PA occlusion time was 79 minutes and 71 minutes, respectively. According to previous experimental studies,16,17 warm ischemia for more than 60 minutes may induce irreversible injury. Consequently, it is possible, though unproven, that prolonged ischemia times > 60 minutes might increase the risk of ARDS. In the future, much more care should be taken to prevent serious respiratory complications.

Conclusion In summary, the surgical technique of PA reconstruction has been more frequently and actively applied for patients with central lung cancer, especially for some patients with lower lobe tumor in our department. It can lead to better quality of life and a stronger longterm survival rate than pneumonectomy. Although the morbidity

Rong Yin et al and mortality is acceptable, surgeons should still pay more attention to some lethal postoperative complications such as bronchopleural fistula and ARDS induced by lung ischemia-reperfusion injury.

Disclosures The authors report no relevant financial conflicts of interest.

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